The Contribution of Microarthropods toAtkk$&knd Food Webs ... · predation by arthropods and vertebrates was reviewed. ... Mesostigmatid mites (Arachnida, Atari) are known to be predators

Am. Mid]. Nat. 148:226-238

The Contribution of Microarthropods to Atkk$&knd FoodWebs: A Review and Model of Belowground ‘Ikansfer in a

Coniferous Forest

JOHN M. JOHNSTON’U.S. EPA, O&u of Research and Lkveiopment, Eqsunts Research Division. 960 cdlcgc Stution Rd.,

Athens, Geotgia 30605

AnsraAcx.-Although beloivground food webs have received much attention, studies con-cerning microarthropods in nondetrital food webs are scarce. because adult oribatid mitesoften number between 250.000-500,000/ m* in coniferous forests, microarthropods are apotential food resource for macroarthropod and vertebrate predators of the forest floor.Although the contribution of microarthropods to aboveground food webs has received littleattention, sufficient data concerning macroarthropods and vertebrate predators were avail-able at the Savannah River Site (SRS, Aiken. South Carolina) to construct a food web modelof the vatious trophic interactions. To supplement this analysis, literature of microarthropodpredation by arthropods and vertebrates was reviewed. This information was incorporatedwith the existing data to produce a model for taxa occurring in coniferous forests at theSRS. because of the diversity and natural history of microartbropod predators, both verte-brate and invertebrate, the resulting web is quite connected and includes transfers to manytrophic levels. The diets of arthropods and vertebrates are variable; yet feeding patterns

reflect the relative abundance of prey at a place and time. Also, many predators feed onmembers of their owngroup. These factors suggest that belowground transfers are deservedof more attention in these and other forest food webs where substantial numbers of detritusfeediig invertebrates inhabit the soil/litter interface and are available as prey items. Moreover, this model can he generalized to describe the dynamics of arthropod and vertebratecommunities in other coniferous forests. The functioning of terrestrial ecosystems is depen-dent upon the interrelationships between aboveground and belowground food webs, andtransfers of biotic components of the decomposer subsystem to aboveground consumersconnect the two subsystems. It is hoped that those consumers traditionally associated withfoliage-based food webs be reconsidered, as they may be gaining a proportion of their nu-trition from organisms in the detrital pathway.

. INTRODUCTION

In forest ecosystems, as in most ecosystems, most net primary productivity flows into thedenital pathway (Coleman and Crossley, 1996). The proportion of flow into the detritalpathway is particularly large in coniferous forests (Knight, 1991). Detrital food webs andtheir trophic interact ions have been s tudied in various systems and models have been proposed that demonstrate the funct ional role of var ious soi l invertebrates in patterns of nu-tr ient cycl ing and decomposi t ion dynamics (Cross ley, 1977; Hunt et a!., 1987; Moore e t uL,

1988; Ingham et uL, 1989; Wardle and Yeates, 1993). Fungi and bacteria form the basalconsumer trophic level of these food webs and are responsible for the majori ty of chemicalbreakdown of p lant mater ia l across a range of ecosystems. Knight (1991) suggested that , inaddition to their role in decomposition in coniferous forests, fungi are also an importantfood source for invertebrates and vertebrates not associated with the belowground system.As a consequence, energy and materials in the detrital pathway are still accessible to above-ground food webs through the production of sporocarps.

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226

228 THEAMERICANMIDLANDNATURALIST 143(l)

bTERATUREtiVIEWAND%JRVEY

In addition to the general ecology and soil biology literature, volumes of Herpetolgiul(Vol. 1-51, spanning 19361995) and theJournal of Hapetobgy (Vol. l-29,1968-1995) werereviewed for diets of reptile and amphibian species that include these microarthropods.Authors that listed “mites” as a group were included, as oribatids are typically the mostabundant constituents of this group. Burton (1976) separated oribatid and nonoribatid preywhen enumerating gut contents of salamanders, and oribatids were more numerous in everyinstance. Records where acarids were lumped under the huger classification of “arachnids”were not included.

Several researchers at the SRS provided information from their research. Jii Hanula(U.S. Forest Service) maintained an extensive macroarthropod pitfall trapping experimenton a range of forest types and successional ages. This trapping, in addition to funnel andflight intercept traps on trees, was implemented to study the abundances and seasonaldynamics of possible food items of the red-cockaded woodpecker (Hanula and Franzreb,1995). Michael Draney (Savannah River Ecology Laboratory, SREL) has been working.withthe Araneae at the SRS for a number of years and contributed information concerningnatural history and significance of roving and soil-dwelling spiders in this system.

ARTHROPOD PREDATOR~OFMICXOARTHROPODS

Mesostigmatid mites (Arachnida, Atari) are known to be predators of both Collembolaand oribatids (Eisenbeis and Wichard, 1987). Pseudoscorpions (Arachnida, Pseudoscorpi-ones) also prey on the microarthopods in general. Their diet consists of Collembola, mitesand nematodes (Eisenbeis and Wichard, 1987). Doubletails (Insecta, Diphua) consume thesmallest soil arthropods (Eisenbeis and Wichard, 1987), though the japygids mainly preyon Collembola (Simon, 1964). Dermaptera (earwigs) are also predators of both of thesemicroarthropods (Gunther and Herter, 1974).

As general& predators, spiders (Arachnida, Araneae) also feed on microarthropod pop-ulations (Wise, 1993). Roving wolf spiders (Lycosidae) are predators of the soil community,and Collembola are one of the main prey groups (Nentwig, 1987). Certain groups areconsidered soil dwellers: purse-web spiders (Atypidae), sack spiders (Clubionidae), tubespiders (Agelenidae) , soil spiders (Halmiidae) and dwarf spiders (Micryphan t&e.). Thesegroups, and others, are likely to feed on microarthropods, though there are apparently nopublished accounts to corroborate this. The relatively small bodied litter dwelling Linyphi-idae are often abundant in the temperate zone and include mites and springtails in theirdiet (Sunderland et d, 1986). Sunderland et al. (1986) found that Collembola accountedfor 99% of the numberof prey caught in their study.

Another arachnid group, harvestmen (Arachnida, Opiliones), catch mites and Collem-bola (among other prey) on the forest floor (Eisenbeis and Wichard, 1987). Martens (1978)recorded Sire duliceriw and 8. rubens burrowing into the soil, sometimes to a depth of 1m, preying on mites and Collembola. Centipedes (Myriapoda, Chilopoda), such as Lithobi;Acspp., prey mostly on small insects. It is likely that these include mites and collembolans(Eisenbeis and Wichard, 1987).

Many beetles (Insecta, Coleoptera) have specific adaptations for capturing microfauna.Some carabids have evolved a successful visual hunting strategy for fast moving prey likeCollembola (Bauer, 1981; 1982a; 1985a). Loriceru piliconis and two species of L&us usemodified seta to enclose a springtail during an attack These traps are constructed fromenlarged seta on the antennae and ventral surfaces of the head (Bauer, 1982b, Bauer, 1985b;Hintzpeter and Bauer, 1986). Larvae of the Scydmaenidae (ant beetles) resemble woodlice

‘2000 JOHNSTON:MICROARTHROPODS 229

and are oribatid specialists. One such species is Cephennium thoracicum, which curls aroundthe captured mite’ and kills by biting with stiletto-like mandibles and injecting it with di-gestive juices. Another species, C. austriacum, picks up mites with its mandibles and caneven walk around carrying the prey (Schuster, 1966a; 1966b).

According to Edward 0. Wilson, ants (Insecta, Hymenoptera) “eat oribatids like popcorn” (in CoIeman and Crossley, 1996). though recorded accounts are rare. In most habitatsant workers are ‘the chief predators of insects and spiders. This is due to the high abundanceand activity of these omnivorous foragers (Hijlldobler and Wilson, 1994). However, somespecies are more efficient predators of microarthropods. For example, ants in the genusAcanthognathus snare springtails with large, trap-like mandibles (Holldobler and Wilson,1994). Masuko (1994) also described the specialized oribatid feeding behavior in two speciesof M~cina M. graminocola ni@onica and M. Java. These small ants-3 mm and 2.5mm long respectively-also accepted entomobryomorph collembolans, beetle larvae (Te-nebrio me&or and Ttibolium con@sum), geophilomorph centipedes and terrestrial amphi-pods (Talitidae) in the laboratory. Masuko (1994) also noted predation on oribatids byAdeknnywnex sp.

VERTEBRATEPREDATORSOFMICROARTHROPODSSpecialization on mites by frogs was evaluated by Simon and Toft (1991). Many small

dendrobatids in the genus Minyobabs consume mites with a higher frequency than expectedbased on the relative frequency of mites compared to the total possible prey fauna. Thereare a number of tropical mite specialists (with % of total number of prey diet in paren-theses): Atdqbus oxyrhynchus (32.2% prey), Pseud@hrytfe curmbomejuveniles (46%) and subadults (25%), Rana aroalis <26 mm (36.6%) and R tempatiu <SO mm (33.4%). Asillustrated by these values, the proportion of small-bodied prey is often much greater forthe smaller frogs and their juvenile stages. In the neotropics mites are the prey equivalentof ants, though at the smalIer end of the size continuum (Simon and Taft, 1991). Theseauthors hypothesize that in the tropics mites are suitable prey for specialists because theyare abundant and slow-moving. An important trade-off, though, is that mites contain ahigher proportion of chitin and are more .difIlcult to ingest. Simon and Toft (1991) alsodemonstrated that mite-eating amphibians are not limited to the neotropics; many occurin North America. Mites were found in 80% of the stomachs of the toad Bufo americanusand made up 16% prey (by number) in S-12 mm size individuals. For another species, B.woodhuusei, mites occurred in 14% of toadlet stomachs (Simon and Taft, 1991). Microar-thropods were found in the diet of the oak toad, B. quercicus, and mites ranked fourth inoverall abundance after ants, beetles and spiders (Hamilton, 1955). Examples of mite-feed-ing by various sizes of hylid frogs are P.wudubs tri&atu (10-15 mm size class, 39% ofstomachs sampled), P nigritu (20-32 mm size class, 11% stomachs sampled) and Acriscrepituns (25-30 mm size class, 12% stomachs sampled) (Simon and Taft, 1991). Otherresearchers have recorded mites and Collembola in the diet of the cricket frog, Ads c)%pituns (Johnson and Christiansen, 1976; Labanick, 1976). Labanick (1976) found that in268 frogs sampled microarthropods made up over 20% of the total number of food items.Labanick (1976) also determined that prey selection was not as important as prey availabilityfor the cricket frog.

Salamanders such as NoqUaJrnus vi&&?scer~ (eastern red-spotted newt) are often vo-racious predators of oribatids and ColIembola and are one of the few species that continueto eat mostly microarthropods as adults (Hamilton, 1932; Burton, 1976; Norton andMacNamara, 1976; MacNamara, 1977). It has been estimated that “a hungry eft may con-sume 2000 springtails” (Behler and King, 1979). The plethodontids (woodland salaman-

2 3 0 THE AMERICAN MIDLAND NATURALIST 143(l)

TABLE I.-Arthropod and vertebrate predators of microarthropods. (Sources: A and M, 1967 =Anderson and Martino, 1967; Draney* = M. Draney, pers. comm.; Edwards = M. L. Edwards, pers.comm.; E and W, 1987 = Eisenbeis and Wichard, 1987; G and S, 1991 = Gibbons and Semlitch, 1991;Hanulat = J. Hanula, pers. comm.; Johnstonf = Johnston, 1996; M and S, 1980 = McMillan andSemlitsch, 1989-N and M, 1976 = Norton and MacNamara, 1976; P and T, 1974 = Powders andTietjen, 1974; S and T, 1991 = Simon and Toft, 1991; Sunderland, 1986 = Sunderland et aL, 1986)

Oribatida Collembola Occurs at S.RS.

Microarthropods

DipluraJapygidaeMesostigmataOpiliones (Harvestmen)Pseudoscorpiones

Macroarthropods

Lithobiidae (Centipedes)Lizhobius sp.Coleoptera (Beetles)Lmicaa QilicornisPselaphidaeP tiliidaeScydmaenidae (Ant lions)

Spiders

LinyphiidaeLycosidae (Wolf spiders)Pardosa sp.Pirata sp.Schizourra sp. (imm.)Hanhniidae

Ants

M)WlWCiW

Reptiles

Tmepene candina

Salamanders

Batrachast$s attmwafusEurycea kmgi~uduNotophthalnw uiridcscensP&hOdan .&+kKusk! ahereusDt?SWg?l4ZthUSjkUSE. bislineataQrinophilus porphyriticusE. quadridig&ata

Frogs

A& cmpitansPseldmis n&daI? tresoiataRana clamitansR s@enoqbhala

E and W, 1987

E and W, 1987E and W, 1987E and W, 1987

Simon, 1964E and W, 1987E and W, 1987E and W, 1987

JohnstonfJohnstontJohnstonfJohnstonfJohnstonf

Eand W, 1987 Johnstonf

Bauer, 1981Park, 1947Riha, 1951Schuster, 1966a,b

HanulafHanulatHanulat

Sunderland, 1986

D-W+Draney*Draney*Dmey*

Draney*

Dmey*Draney*Draney*

D=-P

Masuko, 1994 Hanulat

Edwards C and S, 1991

Adams, 1968A and M, 1967N and M, 1976P and T, 1974Burton, 1976Burton, 1976Burton, 1976Burton, 1976M and S, 1980

Adams, 1968A and M, 1967MacNamara, 1977P and T, 1974Burton, 1976Burton, 1976Burton, 1976Burton, 1976M and S, 1980

G and S, 1991G and S, 1991G and S, 1991

G and S, 1991

M and S, 1980

S and T, 1991S and T, 1991S and T, 1991S and T, 1991S and T, 1991

C and S, 1991G and S, 1991C and S, 1991C and S, 1991G and S, 1991

231

IOribatida C o l l e m b o l a Occun at S.RS.

ToadsBufo terrestris S and T, 1991 G and S, 1991B. qtm-cim Hamilton, 1955 G and S, 1991B. woodhousn’ . ..- S and T. 1991 G and S, 1991

ders) are also microarthropod consumers. Mites and Collembola are consumed regularlyby Batrachoseps at&nuatus (Adams, 1968), Eurycea kmgicauda (Anderson and Martino,1967), Plethodon cinereu.s, Desmognathus J%.SCLU, E . bidineuta, Gyrin0philu.s pgbhyriticus(Burton, 1976) and E. quz&idigi&tu (McMillan and Semlitsch, 1980; Powders and Cate,1980). The relative abundance of the various invertebrates was directly correlated to theproportion of each kind taken by the slimy salamander, Pi&&m glutinosus (Holman,1955). According to Davidson (1956), availability is the single most important factor gov-erning the feeding habits of this species. Comparisons of Plethdm glutirwsus stomach con-tent data from other locations support this assertion. Diets switched apparently from amajority of ants and coleoptera (42% and 18% by biomass respectively) (Davidson, 1956)to diplopods and coleoptera (55% and 8% by biomass) at one site and diplopods, formicidsand chilopods (Sl%, lo%, and 9% by biomass) at yet another (Powders and TieQen, 1974).Burton (1976) was one of the few to distinguish between oribatid and nonotibatid mites inpublished diets; and it $ worth mentioning that in every case oribatids were most numerous,oftenbyamarginofSto1.

A FOOD W EB AT SRS

A synthesis of literature compiled in the present study is summarized in Table 1, and thecited’authority c&inns the presence of each group or species. Many of the invertebrateand+&tkbi$~+xies identified as Oribatida and Collembola predators occur at the SRS.Thk C&&l’rplaiti is esp&&lly diverse with regard to the herpetofkma, and of amphibiansverified as mite feeders in the literature, 13 species occur at the Savannah River Site. In-formation on many taxa is incomplete or n.onexistent, however, and these will be discussed.

Extensive pitfall +ping at SRS revealed that ants are the most numerous animal groupin planted and natural pine stands of a variety of ages (often 90% or more of the totalnumber of arthropods), especially the genera Fktwlepls, Aphaenogas~ Cren@ogasterandSoknu@is (in declining order) (J. Hanula, pers. comm.). Van Pelt (1966) tid Van Pelt andGentry (1985) examined the activity and density of ants in old fields at the SRS, findingDorymyrmex fyramicus to be the most abtidant species and confirming the presence of thegenus Myrmecinu. Dorymymrac &ram.ic~ was a very general feeder that attacks invertebratesand even frogs and toads (Van Pelt, 1966).

The overall effect of ant predation on microarthropods is assumed to be important (Hiill-dobler and Wilson, 1994), but is diicult to state in exact terms. Because of the patchydistribution of ant species, the effect of any one taxon is probably unimportant. However,due to the fact that ants are overall quite numerous, and most carnivorous species consumeroughly the same resources, the net effect of all species can be considerable. Variables thatinfluence the predation intensity of a colony include colony status, season and foragingefficiency. Some ants, such as the tribe Dacetini, are very efficient predators and have amuch greater effect per individual on prey populations than others (R. Carroll, pers.comm.) . In addition to seasonal variation in colony activity, energetic requirements change

.

h. -_‘. /

--._.~ .._ _ . _ . -..- ..-- ---“- -.., -

232 TH E AM E R I C A N MIDLAND N A T U R A L I S T 143(l)

during the lifetime of a colony. Protein requirements are higher in growth phases due todeveloping larvae. The carbohydrate requirements of a colony are higher when i t becomesestabl i shed and requires maintenance instead.

With spiders-the determining factor in prey type is the relative size of the predator.Though the smal ler l inyphi ids eat mites , they are probably not the main d iet . Most ground-dwelling spiders do, however, consume springtails at some stage of development. Adultlycosids (wolf spiders) are unlikely to consume prey as small as springtails, whereas imma-tures may eat little else (M. Draney, pers. comm.). An example of this is the genus Schizocosu,a re la t ive ly abundant lycos id a t the SRS (J. H a n u l a , pers. comm.). Adults of smaller taxathat feed on Collembola include Pardosu, Pi&u (also wandering spiders) and the Hahni-idae.

Beet les are a l so an abhndant , and highly d iverse , group in SRS pine forests (J . Hanula,pers. comm.). Many if not most carabid larvae and adults are opportunistic and polyphagous(saprophages , macrophytophages , carnivores) and may feed on a lmost any so i l invertebrate(Ekschmitt et aZ., 1997) . Most s taphyl in ids are a l so predators o f microarthropods and ma-croartbrpods (Ekschmitt eb aC., 1997) . Not enough natura l h i s tory in format ion i s ava i lab leto make definit ive statements of the impact of coleopteran predators, though their feedingactivities may be considerable (Eisenbeis and Wichard, 1984). For example, Curabus aurutuscan consume up to two and a half times its own body mass. The average daily food con-sumption for a 0 .640 g beet le was 0.875 g (Scherney, 1959; 1961).

With the exception of Terrapne carotina (box turtle), which feeds on invertebrates (Mar-tof et al., 1980), few of the reptile diets have been researched with any degree of detail.Much less i s known about the habi ts of the immature s tages of the same rept i les . Hatchlingturtles feed upon a range of small invertebrates, including Collemhola (M. L. Edwards,pers. comm.), but diets have not been published. This lack of information seems to be abias on the part of herpetologists, rather than a lack of microarthropod feeders in theReptilia, because many species of l izard are both insect ivorous and common to southeasternpine forests. This includes anoles (Adis cardinensir), fence lids (Sc&@cn’~.~ undulatur)and &inks (ScimUu luteralis, Eumems fasciatus, E. inexpectutus and E. l.atiCeps) (Gibbonsand Semli tsch, 1991). Vit t and Cooper (1986) provided the only information in this surveyfor a scincid, Eumms k&c@, and it is one of the few lizards that hunts (mostly for gryllidsand blattids) by actively flushing prey from refugia in the leaf and woody litter. This speciesi s a l so cann iba l i s t i c on all other l izard taxa that i t can manage, due to i t s rather large s izecompared with other &inks (Douglas, 1965). Though adult lizards feed mainly on macro-fauna such as cr ickets , grasshoppers and roaches , the d ie t s of immatures a lmost cer ta in lyinclude microarthropods.

The conclusion reached by many herpetologists i s that diet i s a direct ref lect ion of preyavailability in the environment (Hamilton, 1955; Holman, 1955; Davidson, 1956; Burton,19 ’76 ; Laban ick , 1976 ; Ma&&mar-a, 19’7 ’7) . Though an occas ion4 species may have a spe-cialized diet, a catholic feeding habit is characteristic of most toads, frogs and salamanders.McMillan and Semlitch (1980) found a very dramatic example of this for the dwarf sala-mander, Eurycaa quadrid@tata, in two diierent’sampling locations at the SRS. Mites ac-counted for 24% of the number of prey at one site, while Collembola were taken in hugequantities at another site, numbering several .thousands of individuals (and 97% of the totalprey).

A hypothesized food web is depicted in Figure 1. Information for the remaining predatorsin the system was compiled from a variety of sources. The narrow-mouthed toad (C&m-phryne curolinensis, moved from the genus Microhyla) appears to be an ant specialist, to theextent that some authors labeled it an ectoparasite of ant colonies (Wood, 1948; Holman,

~1-11 ,.-__...., ,” ._.__ .,_,. _ ,... . . , . ., _....A __ .-..z?=_.

2000 JOHNSTON: MICROARTHROPODS 233

FIG. I.-An aboveground food web with belowground connections in a coniferous forest. The posi-tioning and vertical extent of each component corresponds to the various trophic levels for each type.P,@F a@ animal matter of different types and in various stages of decay compose a portion of the

r p@d~+$fpr,f system. Thii material enters the web primarily through the action of ftmgal species.I&% ‘that bbx wid@ (horizontal extent) is for display purposes only and is not meant to imply quali-t&e or quankati~e comparison

.Y

1958). The diet of #ufo WOOdhOUSGi consists mostly of Coleoptera and Hymenoptera (Bushand Menhiiick, 1962). The spadefoot toad, Scaphiophus h. hoUnueki~ feeds primarily onColeoptera and Hymenoptera and Arachnida to a lesser degree (Pearson, 1955). Snakesfeed on a number of salamanders, lizards, frogs, toads and other snakes (Hudson, 1947;Chenoweth, 1948, Orleb, 1951; Healy, 1958; Behler and King, 19’79; Martof d al., 1980;Conant and Collins, 1991). One snake species is known to be an arthropod feeder, thesoutheastern crowned snake TantiUa rxnmuta, and it consumes primarily centipedes as anadult It is also the most frequently captured snake in pitfall traps along drift fences at SRS(Gibbons and Semlitsch, 1991). __

Wild swine (Sus scrofa) feed on soil invertebrates and vertebrates (Singer et a& 1984).Raccoons (hcyon lotor) and the red fox (Vu~ VU&ZS) are also predators of reptiles andamphibians (Schaaf and Carton, 19’70; Skeen et aZ., 1993). Insectivorous birds at the SRSinclude the red-cockaded woodpecker (Picoides &rm!is) and the Carolina wren (Thryotbrus Lu’tiurnus) (Skeen et al., 1993; Hanula and Franxreb, 1995). The broad-winged hawk(Buteo p~!~l$&rus) is a reptile (snake) specialist (Skeen et al., 1993).

A majority of predators--be they invertebrate, amphibian, reptilian or mammalian-areopportunistic feeders on a wide range of prey types and size classes. Patterns of prey con-sumption change not just seasonally but also locally based on availability. This generalization

234 THE AMERICAN MIDLAND NATURALIST 143(l)

likely holds for all such taxa where data were scarce. For the purpose of depicting a foodweb (Fig. 1) this leads to a highly connected web of predators. Many of the groups (ants,spiders, herpetofauna, etc.) prey frequently on members of the same group, and this isdepicted by recycling arrows.

Oribatids are the most numerous microartbropods in forests of the SRS, and ants are byfar the most abundant macroarthropods. A significant transfer of microarthropod biomassthrough the food web appears to be through ant predation. Ants are significant predatorsof arthtopods in general, and these Hymenoptera are sufficiently abundant to be a com-ponent of a variety of vertebrate diets. Quantification of the strength of this link can beachieved only through experimental manipulations of ant abundance. However, most ofthe experimental work to test such aboveground and belowground relationships involvesspiders and Collembola as experimental subjects (see Wise, 1993). The direct and indirecteffects of ant predation on oribatid mites follow a similar reasoning, and the evidence willbe discussed in the following section. Augmentation and removal studies of predators andprey groups could be used to study the trophic effects in this forest ecosystem (in bothdirections) .

Although diets for many likely microarthropod predators were not found in the literature,it is probable that varioui lizard and snake species are indeed making use of microarthro-pods as immatures. Many adult toads, frogs and salamanders consume quantities of antswhen they are abundant. Oribatid mites are even more abundant prey than ants and wouldserve as a likely resource for the smaller herpetofauna and those in early stages of devel-opment. Although information is scarce for this it does seem likely, and the similarity be-tween oribatids and ants as prey types has been suggested (Simon and Toft, 1991).

DISCUSSON

There is evidence to support the conclusion that a considerable proportion of the below-ground biomass in this forest ecosystem is transferred to aboveground predators. Moulderand Reichle (1972) estimated that spiders consumed 44% of the mean annual standingcrop of all soil invertebrates using concentration and turnover rates of radioactive cesiumin a forest floor community. Wise (1993) considers this estimate to be conservative sincemany prey were not “suitable” because of size and palatability. Many others have similarlyconcluded that spiders are important predators in forest ecosystems (Reichle and Crossley,1965; Norton, 19’73; Manley d al., 19’16; Wise, 1993). Ekschmitt et al. (1997) reviewed thepotential of the polyphagous predators, i.e., spiders, carabids and staphylmids, as biologicalcontrol measures in agroecosystems due to their ability to significantly affect the populationdynamics of plant and detrital feeding invertebrates.

There is interest in the indirect effects of forest floor predators as well. However, quan-tifying the effect on belowground communities and the resultant ecosystem processes hasproven to be extremely difficult Rajak et al. (1991) attempted to relate the indirect effectof predator densities (arachnids, carabids, staphylinids and hymenopterans) on decomposition rates and patterns of nutrient cycling (see Wise, 1993). The mechanism of interest tothese authors is the reduction of numbers of de&al feeding invertebrates (e.g., oribatidmites and collembolans) via predation on the soil surface. These authors demonstrated anincrease in decomposition rate in predator exclusion devices with the implication that bothmicroarthropod densities and the rate of decomposition were influenced by spider (andother) predators of the soil/litter interface.

Wise (1993) also reviewed other experimental evidence (e.g., Clarke and Grant, 1968)with regard to the impact of spiders on microarthropod densities. To date, however, no onehas directly manipulated invertebrate predator densities in field experiments and the diE

2000 JOHNSTON: MICROARTHROPODS 235

ficuhies in designing a study to test such an effect are manifold. The design challengesinclude the need for sufficient replication of experimental units (Clarke and Grant, 1968)and the effect of caging predators and their prey (Rajak et UC., 1991). Furthermore, Wise(1993) urged experiments with open controls, larger experimental units and longer dura-tions.

The forests of the Savannah River Site, though an agricuhural crop (plantation), fostera diversity of predator taxa, with a diversity of species in each group. Ekschmitt et al. (1997)offered recommendations for those methods which foster higher abundance and diversityof polyphagous predators in agroecosystems. These include: (1) reduction of agriculturalpractices (e.g., plowing and harvest), (2) maintenance of overwintering sites and (3) theuse of intercropping and mulching (for ‘a diversity of habitat structure and refugia). Inter-estingly, in these managed pine plantations that are harvested every 25 y (on average) thereexists a diversity of ground cover, shrubs, large woody debris, standing dead trees and gapsin canopy cover that are succeeded by hardwood regrowth. Though a passive type of man-agement for the fauna under consideration, it has the effect of supporting an abundantand dynamic community. Summerhayes and Elton (1923) presented one of the few inte-grated food webs that details the feeding interactions between detritivorous microarthropods and aboveground and aquatic biota. In their’Arctic ecosystem, predators of microar-thropods included an arachnid and three species of birds. Clearly, the number of predatorsin the current forest ecosystem results in a greater amount of interaction between thesubsystems as well as more complicated dynamics. As &cussed, the hu.e.rrelatlonship be-tween aboveground and belowground systems has been approached from few directionswith various intents. Food webs can serve as the basis for model development of materialand energetic flows and are appropriate tools for management and decision making. AI-though knowledge of the linkages and strengths of multispecies interactions in a particularsystem is often a prerequisite for better conservation of species, such comprehension hasproven quite diflicult to achieve. There is also the difficulty that the strengths of varioustrophic interactions and even food web membership can change dramatically through time(TavaresQomL ~d~SViUiams, 1996). Though the SRS is one system that has been studiedin some detail, many questions still remain. Moreover, the potential significance of microar-thropod predators will differ as a function of food web composition, season and those taxafavored by the prevailmg type of management. Also, although soil nematodes and enchy-traeid worms have not been d&cussed here, they may also be important components of thedetrital community in aboveground.food webs. The contribution of microarthropods, es-pecially oribatid mites, to aboveground food webs is apparent. Many vertebrates feed onthem directly, and those fauna that prefer larger prey items are often consuming variousarthropod predators of the microfauna. It is hoped that this review stimulates discussion ofthii apparently overlooked, but important, interface between the surface and subsurEdce ofthis, and possibly other, forest ecosystems.

Ackmwts.-The author would like to thank the following individuals for their assistance inthe,form of helpful comments and sharing of their research findings: Ron Carroll (Institute of Ecol-ogy), Mary Lang Edwards (Erskine College), Mike Draney (SREL), J. Whitfield Gibbons (SREL) , JimHanula (U.S.F.S.), Roy Norton (SUNY) and David Walter (Univ. of Queensland). Thii research wasinitiated while the author was completing his Ph.D. Diirtation at the University of Georgia, Instituteof Ecology. The U.S.F.S. Southeast Forest Experiment Station, through a cooperative agreement to theUniversity of Georgia, provided the initial funding for thii work. John Blake, Jim McMinn and MarilynBuford are thanked for their support of this research at the SRS. The comments of M. Craig Barber(U.S. EPA) and two anonymous reviewers improved the manuscript.

THE AM ERICAN M IDLAND NATURALIST

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